Ice‐binding proteins and the ‘domain of unknown function’ 3494 family

Vance, Tyler D. R.; Bayer‐Giraldi, Maddalena; Davies, Peter L.; Mangiagalli, Marco

doi:10.1111/febs.14764

Cited by 49 publications

(47 citation statements)

References 115 publications

(253 reference statements)

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“…The conserved intergenic (spacer) regions lend support to the notion that these regions may serve as transcriptional promoters, as has been postulated for the PCP genes [21,49]. Because the DUF3494 domain in many species has arisen via lateral genetic transfer [59], the presence of these genes in this configuration suggests that they might have arisen via the same mechanism in P. glacialis. Figure 5 shows part of a phylogenetic tree reconstructed with 1080 sequences of available DUF3494 domains encompassing Archaea, Bacteria, and eukaryotes; the complete tree is available as Additional file 4: Supplementary Data 1.…”

Section: Single Evolutionary Origin Of Ice-binding Domains In Dinoflamentioning

confidence: 63%

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Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions

et al. 2020

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Background: Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some can form symbiotic and parasitic associations with other organisms. However, knowledge of the molecular mechanisms that underpin the adaptation of these organisms to diverse ecological niches is limited by the scarce availability of genomic data, partly due to their large genome sizes estimated up to 250 Gbp. Currently available dinoflagellate genome data are restricted to Symbiodiniaceae (particularly symbionts of reef-building corals) and parasitic lineages, from taxa that have smaller genome size ranges, while genomic information from more diverse freeliving species is still lacking. Results: Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. We found that about 68% of the genomes are composed of repetitive sequence, with long terminal repeats likely contributing to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). For each genome, guided using full-length transcriptome data, we predicted > 50,000 high-quality protein-coding genes, of which~40% are in unidirectional gene clusters and 25% comprise single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial origin of ice-binding domains in cold-adapted dinoflagellates. Conclusions: Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Because most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light polar environments. These genomes provide a foundational reference for future research on dinoflagellate evolution.

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Section: Single Evolutionary Origin Of Ice-binding Domains In Dinoflamentioning

confidence: 63%

“…The Pfam domain DUF3494, a known ice-binding domain [59], is over-represented in cold-adapted dinoflagellates [47]. In both P. glacialis isolates (see Additional file 3: Supplementary Table 19), most putative ice-binding genes encode only the DUF3494 domain.…”

Section: Single Evolutionary Origin Of Ice-binding Domains In Dinoflamentioning

confidence: 99%

Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions

et al. 2020

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“…The Pfam domain DUF3494, a known ice-binding domain 52 , is over-represented in coldadapted dinoflagellates 41 . In both P. glacialis isolates ( Supplementary Table 16), most putative ice-binding genes encode only the DUF3494 domain.…”

Section: Single Evolutionary Origin Of Ice-binding Domains In Dinoflamentioning

confidence: 99%

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Stephens

González‐Pech

Cheng

et al. 2019

Preprint

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Dinoflagellates are taxonomically diverse, ecologically important phytoplankton in marine and freshwater environments. Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. For each genome, guided using full-length transcriptome data, we predicted >50,000 high-quality genes. About 68% of the genome is repetitive sequence; long terminal repeats likely contribute to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp).Of all genes, ~40% are encoded unidirectionally, ~25% comprised of single exons. Multigenome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial, origin of ice-binding domains in cold-adapted dinoflagellates. Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Since most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light environments. health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e. 0.12-4.8 Gbp. In comparison, genomes of other free-living dinoflagellates are much larger in size, ranging from ~7 Gbp in the psychrophile Polarella glacialis, to over 200 Gbp in Prorocentrum sp. based on DAPI-staining of DNA content 18 .Repeat content has been estimated at >55% in the genome sequences of some free-living dinoflagellates 19,20 ; single-exon genes have also been described 21 . Given that most dinoflagellate lineages are free-living, whole genome sequences of these taxa are critical to understand the molecular mechanisms that underpin their successful diversification in specialised environmental niches.Polarella glacialis, a psychrophilic (cold-adapted) free-living species, represents an excellent system for genomic studies of dinoflagellates for three reasons. First, it is closely related to Symbiodiniaceae (both in Order Suessiales), the family that contains the coral reef symbionts, e.g. Symbiodinium and related genera. Second, P. glacialis has been reported only in polar regions. Studying the P. glacialis genome can thus provide a first glimpse into molecular mechanisms that underlie both the evolutionary transition of dinoflagellates from a free-living to a symbiotic lifestyle, and the adaptation to extreme environments. Third, the estimated genome size of P. glacialis is still in the smaller range (~7 Gbp 18 ) of all dinoflagellate taxa, which presents a technical advantage in terms of allowing efficient genome assembly and gene prediction.

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“…In addition, most IBPs are secreted and act extracellularly, whereas AFPs act internally. The most common microorganismal IBPs have similar structures based on a ~200-amino acid domain referred to as DUF3494; they are found in bacteria, archaea, algae and fungi (e.g., (9,10)). Other less common IBPs have been identified in a chlorophyte alga (11)(12)(13) and a bacterium (7).…”

Section: Downloaded Frommentioning

confidence: 99%

Ice-Binding Proteins Associated with an Antarctic Cyanobacterium, Nostoc sp. HG1

Raymond

Janech

Mangiagalli

2021

Appl Environ Microbiol

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Ice-binding proteins (IBPs) have been identified in numerous polar algae and bacteria, but so far not in any cyanobacteria, despite the abundance of cyanobacteria in polar regions. We previously reported strong IBP activity associated with an Antarctic Nostoc species. Here, to identify the proteins responsible, as well as elucidate their origin, we sequenced the DNA of an environmental sample of this species, designated Nostoc sp. HG1, and its bacterial community and attempted to identify IBPs by looking for known IBPs in the metagenome and by looking for novel IBPs by MS/MS proteomics analyses of ice affinity-purified proteins. The metagenome contained over 116 DUF3494-type IBP genes, the most common type of IBP identified so far. One of the IBPs could be confidently assigned to Nostoc while the others could be attributed to diverse bacteria, which, surprisingly, accounted for the great majority of the metagenome. Recombinant Nostoc IBPs had strong ice-structuring activities and their circular dichroism spectra were consistent with the secondary structure of a DUF3494-type IBP. Nostoc IBP (nIBP) is unusual in that it is the only IBP identified so far to have a PEP C-terminal signal, a signal that has been associated with anchoring to the outer cell membrane. These results suggest that the observed IBP activity of Nostoc sp. HG1 was due to a combination of endogenous and exogenous IBPs. Amino acid and nucleotide sequence analyses of nIBP raise the possibility that it was acquired from a planctomycete. Importance The horizontal transfer of genes encoding ice-binding proteins (IBPs), proteins that confer freeze-thaw tolerance, has allowed many microorganisms to expand their ranges into polar regions. One microorganism for which nothing is known about its IBPs is cyanobacteria. Here, we identified a cyanobacterial IBP and show that it was likely acquired from another bacterium, probably a planctomycete. We also show that a consortium of IBP-producing bacteria living with the Nostoc contribute to its IBP activity.

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Ice‐binding proteins and the ‘domain of unknown function’ 3494 family

Cited by 49 publications

References 115 publications

Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions

Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Ice-Binding Proteins Associated with an Antarctic Cyanobacterium, Nostoc sp. HG1

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